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Diabetes Metab J 2013;37:140-148
http://dx.doi.org/10.4093/dmj.2013.37.2.140
pISSN 2233-6079 eISSN 2233-6087

DIABETES & METABOLISM JOURNAL

Effects of High Performance Inulin Supplementation


on Glycemic Control and Antioxidant Status in Women
with Type 2 Diabetes
Bahram Pourghassem Gargari1, Parvin Dehghan2, Akbar Aliasgharzadeh3, Mohammad Asghari Jafar-abadi4
Department of Biochemistry and Diet Therapy, Nutrition Research Center, Tabriz University of Medical Sciences,
Student Research Center, Faculty of Health and Nutrition, Tabriz University of Medical Sciences,
3
Endocrine and Metabolism Section, Imam Reza Teaching Hospital, Faculty of Medicine, Tabriz University of Medical Sciences,
4
Department of Statistic and Epidemiology, Faculty of Health and Nutrition, Tabriz University of Medical Sciences, Tabriz, Iran
1
2

Background: The purpose of this study was to evaluate the effects of high performance inulin supplementation on blood glycemic control and antioxidant status in women with type 2 diabetes.
Methods: In a randomized, triple-blind controlled trial, 49 females (fiber intake <30 g/day, 25<body mass index<35 kg/m2)
with type 2 diabetes were recruited from the Iran Diabetes Society and from endocrinology and metabolism clinics associated
with the Tabriz University of Medical Science. The participants were divided into one of two groups in which the participants either received 10 g/day of inulin (intervention, n=24) or maltodextrin (control, n=25) for 2 months. Fasting blood samples were
obtained and both glycemic control and antioxidant status were determined at baseline and at the end of the study.
Results: At the end of the study period, there were significant decreases in fasting plasma glucose (8.47%), glycosylated hemoglobin (10.43%), and malondialdehyde (37.21%) levels and significant increases in total antioxidant capacity (18.82%) and superoxide dismutase activity (4.36%) in the inulin group when compared to the maltodextrin group (P<0.05). Changes in fasting
insulin, homeostasis model assessment of insulin resistance, and catalase activity were not significant in the inulin group when
compared with the maltodextrin group. Glutathione peroxidase activity remained unchanged in both groups.
Conclusion: Inulin supplementation may improve some glycemic and antioxidant indices and decrease malondialdehyde levels
in women with type 2 diabetes. Further investigations are needed in order to confirm the positive effects that inulin may have on
the glycemic and antioxidant indices of patients with type 2 diabetes.
Keywords: Antioxidants; Diabetes mellitus, type 2; Insulin resistance; Inulin; Malondialdehyde

INTRODUCTION
Diabetes mellitus (DM) is a common health problem and is the
main cause of morbidity in developing and developed countries. The number of people with diabetes is gradually increasing, and its prevalence was reported to be 171 million people in
2000. It is estimated that at least 366 million people will suffer
from DM by the year 2030 [1]. In 2010, the prevalence of DM
was 8% and its health expenditure was equal to 600 million
Corresponding author: Parvin Dehghan
Student Research Center, Faculty of Health and Nutrition, Tabriz University
of Medical Sciences, Attar Nishaboori St., Golghasht St., Tabriz 51664, Iran
E-mail:dehghan.nut@gmail.com
Received: Sep. 19, 2012; Accepted: Jan. 3, 2013

U.S. dollars in the country of Iran [2]. DM is a metabolic disease that is characterized by the existence of hyperglycemia
along with having biochemical alterations of glucose, lipid profile, lipid peroxidation, insulin resistance and -cell dysfunction [3]. Prolonged exposure to hyperglycemia causes oxidative
stress and an imbalance of the oxidant/antioxidant status. Oxidative stress has been suggested to play a key role in the pathophysiology of type 2 diabetes and its complications [4].
Nowadays, functional foods are of interest due to their poThis is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/)
which permits unrestricted non-commercial use, distribution, and reproduction in any
medium, provided the original work is properly cited.

Copyright 2013 Korean Diabetes Association

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Inulin and biochemical indices in T2DM women

tential health benefits [5]. The potential consequence of oxidative stress could be attenuated by the dietary consumption of
functional foods. Inulin-type fructans, a well-defined type of
functional foods, are naturally found in vegetables and fruits
such as: onions, garlic, chicory root, banana, and wheat, and
are used as prebiotic and dietary fiber in various food items.
Inulin-type fructans are indigestible carbohydrates, contain
fructose monomers that are linked by (12) bounds, and are
arranged as nonviscous, soluble, and fermentable fibers. High
performance (HP) inulin is a prebiotic that has a long-chain,
high-molecular weight mixes of inulin-type fructans, without
any fructans that have a degree of polymerization <10 [5].
This type of inulin is incorporated into baked goods, milk
products, drinks, and desserts as a substitute for sugar and/or
fat [6]. HP Inulin has a specific colonic fermentation property
that is able to change the composition of the gut microflora toward bifidobacteria. Ingestion of 5 to 8 g/day of inulin should
be sufficient to exhibit a positive effect on the gut microflora.
Possible side effects of inulin-type fructans can be seen at doses that are higher than 20 g/day [5].
The effects that inulin-type fructans have on reducing blood
glucose and oxidative stress has been shown in previous animal based studies [7,8]. To our knowledge, all of the human
studies to date have only assessed the effects of fructooligosaccharides (FOS), which have a lower molecular weight than HP
inulin, on diabetic patients and that there has been no study
that has yet assessed the effects of HP inulin on diabetic patients [9-11]. The results of the FOS studies on diabetic patients have been inconsistent. Yamashita et al. [9] has shown
that beneficial effects of oligofructose exist in regards to the
blood glucose and lipid profile of diabetic patients. In contrast,
a couple of other studies have failed to show any beneficial effects of inulin-type fructans in diabetic patients [10,11]. Due
to the probably beneficial effects of inulin-type fructans, especially on the carbohydrate metabolism [9, 12] and the antioxidant status [7,8], and the scarcity of data that exist on the
HP inulin effect on glycemic and antioxidant status, the present study was designed to assess the hypoglycemic and antioxidant effects of HP inulin in women with type 2 diabetes.

METHODS
Subjects
Sixty-five females with DM that were between the ages of 20
and 65 years of age had participated in the study. Participants
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were recruited from the Iranian Diabetic Society and from endocrinology and metabolism clinics that were associated with
the Tabriz University of Medical Science. Inclusion criteria
was defined as: having DM for more than 6 months, currently
having anti-diabetic treatment, having a stable diet and a body
mass index (BMI) >25 kg/m2 for the past 3 months. DM was
defined as having a fasting glucose level that is 126 mg/dL
[13]. Subjects were excluded if they had a history of gastrointestinal, pancreatic, or cardiovascular disease, renal, thyroid or
liver disturbance, being pregnant or lactating, consuming prebiotics, or probiotics, antibiotics, antacids, alcohol, antidiarrheal, anti-inflammatory or laxatives drugs, or lipid-lowering
medications 2 months prior to the intervention or during the
intervention, or if the individual had a typical fiber intake >30
g. Prior to the intervention, an appointment time was set for
each subjects to provide study information and to complete
their individual questionnaire and to provide their written informed consent. Demographic data including age, medication, and diabetes duration (in years) was obtained by using
the questionnaire. The study was approved by the Ethical
Committee of the Tabriz University of Medical Sciences and it
was registered on the Iranian Registry of Clinical Trials website (http://www.irct.ir/, IRCT201110293253N4).
Experimental design
The randomized control trial design was used to perform our
study in parallel and as a triple-blinded study. Both the participants and the researcher were blinded to the intervention.
Participants were randomly assigned in to one of two groups
by using a block randomization procedure, which matched
subjects to each block based on BMI and age. The experimental group received a daily supplement of 10 g of HP inulin
(Sensus, Roosendaal, The Netherlands) and the control group
received a similar amount of maltodextrin (Jiujiang Hurirong
Trade Co., Ltd, Jiujiang, China), which served as the placebo,
for 2 months. Daily supplements were divided in to two packages of 5 g each, which were instructed to be consumed with
breakfast and dinner along with a cup of water. The taste and
appearance of maltodextrin and inulin were similar to one another and the substrates were provided to the volunteers in
similar opaque packages. Subjects received half of their packages at the beginning of the study and received the remaining
packages in the middle of the study. In order to minimize the
dropout rate and to ensure the consumption of the supplements, the participants received a phone call once per week.

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Gargari BP, et al.

The phone number of the researcher was provided to all of the


participants to help answer any question or concerns that may
arise throughout the intervention. Subjects were recommended to return all of their packets regardless of whether they
were (full or empty) in order to assess the consumption status
of each participant. The volunteers were recommended to
have stable physical activity throughout the duration of the
study. A diagram of the study design is shown in Fig. 1.
Body weight and food intake assessment
A research assistant measured the anthropometric indices, including body weight and height, at the beginning and at the
end of the trial. Weight was measured to the nearest 0.1 kg,
and the height was measured, to the nearest 0.1 cm. BMI was
calculated as weight in kilograms divided by the square of the
height in meters. Nutrient intake data was also collected at the
beginning and at the end of the trial period. Diet evaluations
were performed with the use of 3-day diet record at the baseline and at the end of the study. All of the subjects attended a
training meeting prior to the start of the intervention where
they were instructed on how to properly use the food scale and
record their food intake. Subjects were instructed to report all
of the food they had consumed for 2-week days and 1-weekend day at the beginning and at the end of the study. Dietary
data were analyzed using the Nutritionist 4 software (First Databank Inc., Hearst Corp., San Bruno, CA, USA).
65 Women assessed for
eligibility
11 Did not meet the criteria
for study
54 Randomized

27 Inulin group

2 Did not consume the


supplement according
to the plan

2 Medication change
1 Moved

24 Completed

Fig. 1. Study design.

142

27 Placebo group

25 Completed

Blood sampling and biochemical assays


At the beginning and at the end of the trial period, 10 mL of
venous blood were collected between 7:00 to 9:00 AM after an
overnight fast, into two vacutainer tubes, in which one tube
contained ethylene-diamine-tetraacetic acid in order to measure the blood levels of glycosylated hemoglobin (HbA1c) and
the other tube contained sodium fluoride in order to determine glucose, insulin and antioxidant indices including the
total antioxidant capacity (TAC), superoxide dismutase
(SOD), glutathione peroxidase (GSH-Px), catalase, and malondialdehyde (MDA). The serum and plasma samples were
separated from whole blood by centrifugation at 2,500 rpm for
10 minutes (Beckman Avanti J-25; Beckman Coulter, Brea,
CA, USA) at room temperature. The serum samples were
stored at -20C immediately after centrifugation until they
were used for their respective assays. Fasting plasma glucose
(FPG), HbA1c, and insulin were analyzed on the day of sampling. FPG was measured by using the enzymatic method using an Abbot Model Aclyon 300, USA autoanalyzer with kits
from Pars-Azmone (Tehran, Iran). HbA1c was determined
using the sample of whole blood by using an automated HP
liquid chromatography analyzer with commercially available
kits from Bio-Rad D-10 Laboratories, Schiltigheim, France.
Serum insulin was measured using the chemiluminescent immunoassay method (LIAISON analyzer 310360; Diasorin
S.P.A, Verecelli, Italy).
Homeostasis model assessment of insulin resistance (HOMAIR) was calculated according to the following formula: [fasting
insulin (U/mL)FPG (mg/dL)]/405 [14]. Measurement of
TAC in serum and SOD and GSH-Px in whole blood was performed by using the colorimetric method with commercial kits
(TAS, RANDOX kits; SOD, RANSOD kits; and GSH-Px, RANSEL kits; RANDOX Laboratory, Crumlin, UK), on an automatic
analyzer (Abbott model Alcyon 300; Abbott Laboratories, Abbott Park, IL, USA). The serum MDA level, which is used as a
marker for lipid peroxidation and oxidative stress, was measured
by using a reaction with thiobarbituric acid (TBA) as a TBA reactive substance (TBARS) in order to produce a pink colored
complex. This fluorescence intensity was measured at 547 nm
with an excitation at 525 nm with a spectrofluorimeter (model
SFM 25A; Kontron, Milan, Italy) [15]. Catalase activity was estimated using the method described by Aebi [16]. Catalase can
degrade H202 and this can be measured directly by the reduction in the absorbance at 240 nm. The H202 was diluted with
phosphate buffer that was at a pH 7.0 and its initial absorbance
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Inulin and biochemical indices in T2DM women

was adjusted between 0.5 to 0.6 absorbance units at 240 nm. The
reduction in the absorbance was measured. One unit of catalase
activity was defined as the amount of catalase that is fully absorbed in 30 seconds at 25C. The catalase activity was then calculated from the change in absorbance and was finally expressed
as units per milliliter [16].
Statistical analysis
Data were analyzed using the SPSS software version 17.0 (SPSS
Inc., Chicago, IL, USA). The results were expressed as mean
standard deviation. The normality of the distribution of data
was evaluated by the one-sample Kolmogorov-Smirnov test. For
quantitative variables, paired and unpaired sample t-tests were
used for means comparisons. The medications used in the two
groups were compared using the Mann-Whitney U test. Analysis of covariance (ANCOVA) was used to identify any differences between the two groups after intervention, and was adjusted for the baseline measurements and covariates. Differences
with a P<0.05 were considered to be statistically significant.

RESULTS

Effect of inulin supplementation on body weight and


dietary intakes
The comparisons between the two groups showed that there
were no significant differences in regards to the baseline body
weight and the BMI (Table 1). The dietary intake of the macronutrients is shown in Table 2. The comparison between the
baseline dietary intakes of the two groups showed that there
was no significant differences in the energy or the macronutrients intake, with the exception of dietary fiber which was significantly higher in the maltodextrin group.
After 2 months of supplementation, the body weight and
BMI remained unchanged in the maltodextrin group, while
both the body weight and BMI significantly decreased in the
inulin group (75.40 11.31 to 72.85 11.16, 31.60 4.09 to
30.504.02, respectively; P<0.05). These changes were significant in the inulin group when compared to the baseline values
(P<0.05). Intakes of energy, carbohydrate and total fat were
significantly different between the two groups at the end of the
study. In the inulin group the intake of energy and the total fat
decreased significantly, while in the maltodextrin group they
remained unchanged.

Of the 65 participants that were assessed for study eligibility,


49 of the participants completed the study (inulin group, 24;
placebo group, 25) (Fig. 1). Participants did not report any adverse effects or symptoms with the inulin supplementation.
Table 1 shows the baseline characteristics of the participants in
the two groups. The two groups were similar in their initial
characteristics.

Effects of inulin supplementation on glycemic indices and


oxidative stress parameters
At the beginning of the study, there were no significant differences between the inulin group and the maltodextrin group in

Table 1. Baseline characteristics of the study participants

Variable

Period

Maltodextrin
(control)
group (n=25)

Inulin
group (n=24)

Initial

1,770.17205.60

1,693.60250.57

End

1,798.23238.95

1,417.86236.70a,b

Initial

224.7147.93

203.0064.31

End

223.3137.40

175.9250.34b

Initial

54.8511.86

51.2515.23

End

55.3314.70

54.2312.18

Initial

52.9113.34

54.3112.15

End

51.8314.91

45.628.70a,b

Initial

18.356.62

10.604.60c

End

14.923.95

12.954.30

Table 2. Daily dietary intake of participants at baseline and the


end of the study

Maltodextrin
(control)
group (n=25)

Inulin
group (n=24)

Energy, kcal

Age, yr

48.699.74

47.7710.14

Carbohydrate, g

Weight, kg

70.5311.05

75.4011.31

Characteristic

Height, cm

153.506.50

154.405.82

BMI, kg/m2

29.904.24

31.614.09

Diabetes duration, yr

5.334.60

7.335.42

Metformin 500 mg, tablets/day

2.710.94

2.851.08

Glibenclamide 5 mg, tablets/day

1.961.17

2.290.99

Values are presented as meanstandard deviation. For all characteristics, there were no significant differences between the maltodextrin
and inulin groups (all P>0.05, based on independent samples t-tests).
BMI, body mass index.
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Protein, g
Total fat, g
Dietary fiber, g

Values are presented as meanstandard deviation.


a
P<0.05, paired t-test, bP<0.05 analysis of covariance adjusted for dietary fiber and baseline values, cP<0.05, unpaired t-test.

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regards to the glycemic indices and the oxidative stress parameters (Tables 3 and 4). At the end of the study, there was a significant decrease in the FPG (8.47%), HbA1c (10.43%), and
MDA (37.21%) in the inulin group when compared to that of
the maltodextrin group (P<0.05, ANCOVA when adjusted for
dietary fiber, energy changes, weight changes, and baselines
values). We observed no significant reduction in the fasting
insulin (34.32%) or the HOMA-IR (39.48%) in the inulin
group when compared to the maltodextrin group (P>0.05,
analysis of the covariance when adjusted for dietary fiber, energy changes, weight changes, and baselines values).
Inulin supplementation caused a 18.82% increase in the
TAC and a 4.36% increase in the SOD when compared with
the maltodextrin group after adjusting for dietary fiber, energy
changes, weight changes and baselines values (P<0.05). The
TAC levels increased (0.850.15 to 1.010.17 mmol/L) and
the MDA levels decreased (3.751.81 to 2.701.50 nmol/mL)
in the inulin group (P<0.05). Levels of catalase increased in
the inulin group (P<0.05, paired t-test), but this change was
not significant when compared to that of the maltodextrin
group (P>0.05, ANCOVA adjusted for dietary fiber, energy
changes, weight changes, and baseline values). GSH-Px activity remained unchanged in both groups. In the maltodextrin
group the TAC, MDA, SOD, and catalase changes that were
observed were not significant.
Table 3. Effects of 2 months of inulin or maltodextrin supplementation on glycemic indices in studied subjects
Variable

Period

Maltodextrin
(control)
group (n=25)

FPG, mg/dL

Initial

157.7610.60

161.6815.10

End

156.1214.17

146.6019.90

Initial

8.200.94

8.400.94

End

8.301.09

7.700.69a,b

HbA1c, %

Fasting insulin, U/mL Initial

HOMA-IR

Inulin
group (n=24)

a,b

13.163.80

14.034.30

End

13.444.80

9.293.20a

Initial

5.151.60

5.602.00

End

5.201.60

3.401.40

a
a

Values are presented as meanstandard deviation.


FPG, fasting plasma glucose; HbA1c, glycosylated hemoglobin; HOMAIR, homeostasis model assessment of insulin resistance.
a
P<0.05, paired t-test, bP<0.05 analysis of covariance adjusted for dietary fiber, energy changes, weight changes, and baseline value.

144

DISCUSSION
High fiber diets can be beneficial in the prevention and management of diabetes. Some studies have reported that prebiotic
fibers may have a dominant effect on the control of diabetes
[17]. Therefore, in this clinical trial, we investigated the effect
that HP inulin supplementation has on glycemic indices and
on antioxidant markers of type 2 diabetic patients. Our results
showed that two months of HP inulin supplementation significantly decreased body weight and BMI when compared to the
group that received maltodextrin supplementation. Similar results have been shown with oligofructose supplementation in
animal studies and in studies with diabetic patients [11,18,19].
Parnell and Reimer [20] have reported that the supplementation of healthy adults with oligofructose at a dose of 21 g/day
for 12 weeks decreased body weight. In our study, the energy
intake of the inulin group significantly decreased (1,693.60
250.57 to 1,417.86236.70, P<0.05). The exact mechanism(s)
of weight reduction by inulin remains unclear. Some gut satiety hormones, especially those that are responsive to diet composition, including glucagon-like peptide 1 (GLP-1), PYY, and
ghrelin, are proposed to influence weight reduction [21].
In order to consider weight reduction as a main intervenTable 4. Effects of 2 months of inulin or maltodextrin supplementation on the antioxidative indices and MDA in studied
subjects
Variable

Period

Maltodextrin
(control)
group (n=25)

Inulin
group (n=24)

TAC, mmol/L

Initial

0.890.10

0.850.15

End

0.850.19

1.010.17a,b

SOD, U/mg Hb
GSH-Px, U/g Hb
Catalase, U/g Hb
MDA, nmol/mL

Initial

1,599.64138.15

1,566.18128.87

End

1,580.00144.55

1,648.97139.07a,b

Initial

33.402.62

33.202.42

End

33.312.80

33.702.60

Initial

66.5017.70

59.9217.40

End

65.0118.37

72.9526.02a

Initial

3.771.24

3.751.81

End

4.301.90

2.701.50a,b

Values are presented as meanstandard deviation.


MDA, malondialdehyde; TAC, total antioxidant status; SOD, superoxide dismutase; GSH-Px, glutathione peroxidase.
a
P<0.05, paired t-test, bP<0.05 analysis of covariance adjusted for dietary fiber, energy changes, weight changes, and baseline values.
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Inulin and biochemical indices in T2DM women

tional cause of observed changes in studied biochemical parameters, we included it in the ANCOVA model as a confounding factor. After the adjustment for weight reduction,
and energy intake, we showed that 2 months of inulin supplementation reduced the FPG, HbA1c, fasting insulin, and
HOMA-IR when compared to that of the maltodextrin group.
There were no statistically significant differences in the fasting
insulin and HOMA-IR between the two groups.
To the best of our knowledge there have not been any studies to date on the HP inulin effects in diabetic patients and
there have only been three studies that have investigated the
effects of fructans other than HP inulin on glucose and insulin
in type 2 DM patients [9-11]. Yamashita et al. [9] have shown
that oligofructose supplementation at a dose of 8 g/day for 2
weeks decreased the FPG levels in type 2 DM patients. Luo et
al. [10] and Alles et al. [11] have reported that there were no
significant changes that were observed with oligofructose supplementation, on FPG fasting insulin in patients with type 2
DM.
Jackson et al. [22] and Giacco et al. [23] have shown that
prebiotic supplementation (10 g/day inulin for 8 weeks in
healthy subjects and 10 g/day of short-chain-fructo-oligosaccharides for 2 months in individuals with mild hypercholesterolaemia, respectively) decreased fasting insulin. Russo et al.
[24] have reported that a significant decrease in HbA1c and
HOMA-IR in healthy young volunteers can be achieved by introducing inulin-enriched pasta. The different results obtained
in these studies may be explained by the dose and the kind of
supplementation, pathologic state and basal levels of the glycemic indices of the type 2 DM patients being studied.
Several mechanisms have been proposed to explain the hypoglycemic effect of fibers. Soluble fibers, such as inulin, can
control or lower serum glucose by delaying gastric emptying,
retarding entry of glucose into the blood stream, and reducing
the post-meal rise of serum glucose [25]. Also, the modification of the secretion of the gut hormones such as GLP-1 [26]
and short-chain fatty acids (SCFA), which are produced from
colonic fermentation of prebiotics [27], can affect serum glucose and insulin levels. SCFA may play a role in the so-called
ileocolonic brake, which explains the inhibition of gastric
emptying when nutrients reach the ileocolonic junction [27].
Oligofructose also increases glucose tolerance with increasing
levels of GLP-1, plasma insulin, pancreatic insulin, and -cell
mass [19], as well as an increase of GLP-2 [18].
Lipid peroxidation is higher in type 2 DM patients. Reduced
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lipid peroxidation and improved antioxidant status might be


one of the mechanisms that may prevent and treat diabetic
complications [28]. MDA is the main product of polyunsaturated fatty acids peroxidation in cells. MDA is a good marker
of oxidative stress [29]. There are antioxidant systems that fight
free-mediated damage. Antioxidant systems involve enzymes
such as SOD, catalase, and GSH-Px as well as nonenzymatic
substances such as vitamins and GSH [30].
There is consistent evidence that the total antioxidant status
in type 1 or 2 DM is lower than that of age-matched controls
[28]. We found significantly decreased levels of serum MDA
in the inulin group when compared to that of the maltodextrin group. Also, our study showed that inulin supplementation significantly increased the TAC levels and SOD activity.
Catalase levels increased in the inulin group (P<0.05, paired ttest), but it was not different when compared to the maltodextrin group (P>0.05, unpaired t-test). The activity of GSH-Px
did not significantly change in either group.
According to the review of the existing literature, there have
been no studies on the effect that inulin may have on the antioxidant status of type 2 DM patients, and so we have reported
the results of some similar studies. Wang et al. [31] have
shown that 5% of xylooligosaccharides increase the activity of
catalase, SOD, and GSH-Px and decreased MDA in rats. Rishi
et al. [30] have shown that the activity of SOD and glutathione
increased in mice treated with probiotics in conjunction with
a prebiotic and observed a decrease in the activity of MDA.
Baynes [32] has suggested that the supplementation of xylooligosaccharides reduces the activity of catalase and that it did
not change the activity of SOD and GSH-Px in type 2 DM patients. Gourineni et al. [33] have reported that dietary bioactive compounds such as prebiotics, their byproducts, and metabolites may increase the activity of glutathion-S-transferase,
catalase, and SOD in prebiotic (synergy1)-fed mice. These results are in agreement with the results of our study.
Conversely, Seidel et al. [34] have reported that the consumption of bread that is supplemented with inulin did not
significantly change the ferric reducing ability of plasma in
male smokers and nonsmokers. Another study on the supplementation with inulin and FOS shows that there is no affect on
serum TAC, GSH-Px, and SOD activities, while it decreases
TBARS in rats [7]. Kozmus et al. [8] have reported that dietary
supplementation with dextrin or oligofructose leads to a 20%
decrease in total glutathione and reduced glutathione (GSH).
The activities of glutathione dependent antioxidant enzymes,

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Gargari BP, et al.

SOD, catalase, and MDA remain unchanged in the dextrin or


oligofructose groups [8]. These different results may be related
to dose and type of prebiotic, species, genotype of subject, basal antioxidant, and glycemic status, and pathologic state of the
subjects.
The exact mechanisms of the fructans antioxidant properties
remain unclear. Further research studies should be designed in
order to obtain a precise perception of the mechanism(s) that
are responsible for these potential beneficial effects of fructans
against the complications of diabetes. Inulin-type fructans may
act as antioxidant themselves and, they could act directly as reactive oxygen species (ROS) that indirectly scavenge through
SCFAs and antioxidant enzymes [35]. One of the possible
mechanisms is the prebiotics ability to modify microflora in
the gastrointestinal tract. Gobinath et al. [36] have shown that
the consumption of prebiotics, such as oligosaccharides and
xylo-oligosaccharides, stimulate the growth of bifidobacteria
and lactobacicilli. Lactic acid bacteria have SOD and in vitro
studies have shown that lactic acid per se and the fermentations of FOS by deferent strains of bifidobacteria lead to the
elimination of free radicals [37]. Also, it may be that lactobacilli
resident in gut lyses and release their intracellular antioxidative
constituents that in turn help to decrease the MDA [31]. Another possible mechanism may be due to the ability of prebiotics to modify gene expression of antioxidant enzymes. It is reported that the consumption of chicory reduces oxidative
stress, restores GSH levels and induces gene expression, which
results in the overexpression of the activity of the antioxidant
enzyme catalase and in turn, up-regulating the endogenous
antioxidant defense system [38]. It has been suggested that the
consumption of inulin supplementation exerts these same systemic antioxidative effects in the colon. It is known that enhanced concentrations of butyrate in colonic cells results in reduced colonic myeloperoxidase activity and restored GSH
concentration. Also, butyrate has been effective in controlling
the enhancement of ROS levels and in decreasing ROS-mediated p42/44 MAPK phosphorylation [39]. Another mechanism that may have contributed to the antioxidant indices is
the lowering of the formation of advanced glycation end products (AGEs). Increased blood glucose levels could be due to
oxidative stress and this would results in the formation of AGE
products. It is suggested that the dietary oligosaccharides may
reduce the oxidative stress by reducing the formation of these
AGE products [38].
Our study did have some limitations, including a small sam-

146

ple size and a short intervention time. We did not measure serum fatty acids or take into consideration the glucose clamp.
We also did not define gut microflora changes with inulin supplementation. Measuring of other oxidative stress indices, such
as F2-isoprostanes, could strengthen the results of our study.
In conclusion, the results of this study showed that inulin
supplementation reduces body weight and improves glycemic
indices, antioxidant indices, and the MDA levels in type 2 DM
patients. These findings suggest a safe and inexpensive intervention for the management of type 2 DM. Further investigations are needed in order to confirm the positive effect that inulin had on the glycemic and antioxidant indices and the
MDA in type 2 DM patients.

CONFLICTS OF INTEREST
No potential conflict of interest relevant to this article was reported.

ACKNOWLEDGMENTS
The authors would like to thank all of the patients for their
participation in this study. They would also like to thank Mr.
Firuz Purrahim for his help in recruiting these participants
and also to Mr. Amir M. Vatankhah for his technical assistance throughout this project. This research project was also
financially supported by the Health and Nutrition Faculty of
the Nutrition Research Center and the Vice Chancellor of Research of the Tabriz University of Medical Sciences in Iran.
This article was written based on the data from a PhD thesis
on nutrition, which was registered in the Tabriz University of
Medical Sciences.

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